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TIP Revista Especializada en Ciencias Químico-Biológicas

2022, Number 1

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TIP Rev Esp Cienc Quim Biol 2022; 25 (1)

Regulatory mechanisms controlling the expression of flagellin in bacteria

Benítez JM, Camarena L

Language: Spanish
References: 88
Page: 1-12
PDF size: 415.89 Kb.


ABSTRACT

Over the last few years, great breakthroughs have been made in the study of the structure and regulation of the bacterial flagellum. Despite their diversity, all flagellar systems share a basal body, a hook, and a filament. The flagellar assembly is tiered and tightly regulated. The final step in the flagellar biogenesis is the filament assembly composed by flagellin subunits, the most abundant flagellar protein. The filament synthesis is metabolically expensive hence, is tightly regulated. In this review, we present the most relevant advances in the understanding of the regulatory mechanisms of flagellin expression at the transcriptional, posttranscriptional, and posttranslational level across the most representative bacterial groups.


REFERENCES

  1. Aldridge, P. D., Karlinsey, J. E., Aldridge, C., Birchall, C.,Thompson, D., Yagasaki, J. & Hughes, K. T. (2006). Theflagellar-specific transcription factor, σ28, is the Type IIIsecretion chaperone for the flagellar-specific anti- σ28factor FlgM. Genes and Development, 20(16), 2315–2326.https://doi.org/10.1101/gad.380406

  2. Anderson, D. & Newton, A. (1997). Posttranscriptionalregulation of Caulobacter flagellin genes by a lateflagellum assembly checkpoint. Journal of Bacteriology,179(7), 2281–2288. https://doi.org/10.1128/jb.179.7.2281-2288.1997

  3. Anderson, P. & Gober, J. (2000). FlbT, the post-transcriptionalregulator of flagellin synthesis in Caulobacter crescentus,interacts with the 5’ untranslated region of flagellinmRNA. Molecular Microbiology, 38(1), 41–52. https://doi.org/10.1046/j.1365-2958.2000.02108.x

  4. Ardissone, S., Kint, N., Petrignani, B., Panis, G. & Viollier, P. H.(2020). Secretion Relieves Translational Co-repression bya Specialized Flagellin Paralog. Developmental Cell, 55(4),

  5. 500-513.e4. https://doi.org/10.1016/j.devcel.2020.10.0055. Ardissone, S., Kint, N. & Viollier, P. H. (2020). Specificity inglycosylation of multiple flagellins by the modular and cellcycle regulated glycosyltransferase flmg. ELife, 9, 1–28.https://doi.org/10.7554/eLife.60488

  6. Arnosti, D. N. & Chamberlin, M. J. (1989). Secondary σ factorcontrols transcription of flagellar and chemotaxis genes inEscherichia coli. Proceedings of the National Academy ofSciences of the United States of America, 86(3), 830–834.https://doi.org/10.1073/pnas.86.3.830

  7. Barembruch, C. & Hengge, R. (2007). Escherichia coli arecontrolled by FlgM-modulated proteolysis. MolecularMicrobiology, 65(1), 76–89. https://doi.org/10.1111/j.1365-2958.2007.05770.x

  8. Beeby, M. (2015). Motility in the epsilon-proteobacteria.Current Opinion in Microbiology, 28, 115–121. https://doi.org/10.1016/j.mib.2015.09.005

  9. Belas, R., Horikawa, E., Aizawa, S. I. & Suvanasuthi, R. (2009).Genetic determinants of Silicibacter sp. TM1040 motility.Journal of Bacteriology, 191(14), 4502–4512. https://doi.org/10.1128/JB.00429-09

  10. Bertero, M. G., Gonzales, B., Tarricone, C., Ceciliani, F. &Galizzi, A. (1999).Overproduction and characterizationof the Bacillus subtilis anti-sigma factor FlgM. Journal ofBiological Chemistry, 274(17), 12103–12107. https://doi.org/10.1074/jbc.274.17.12103

  11. Blum, T. B., Filippidou, S., Fatton, M., Junier, P. & Abrahams, J.P. (2019). The wild-type flagellar filament of the FirmicuteKurthia at 2.8 Å resolution in vivo. Scientific Reports, 9(1),1–8. https://doi.org/10.1038/s41598-019-51440-1

  12. Calvo, R. & Kearns, D. (2015). FlgM Is secreted by theflagellar export apparatus in Bacillus subtilis. Journalof Bacteriology, 197(1), 81–91. https://doi.org/10.1128/JB.02324-14

  13. Campbell, B., Engel, A. S., Porter, M. L. & Takai, K. (2006).The versatile ε-proteobacteria: Key players in sulphidichabitats. Nature Reviews Microbiology, 4(6), 458–468.https://doi.org/10.1038/nrmicro1414

  14. Caramori, T., Barillà, D., Nessi, C., Sacchi, L. & Galizzi, A.(1996). Role of FlgM in σD-dependent gene expression inBacillus subtilis. Journal of Bacteriology, 178(11), 3113–3118. https://doi.org/10.1128/jb.178.11.3113-3118.1996

  15. Chadsey, M., Karlinsey, J. & Hughes, K. (1998). The flagellaranti-σ factor FlgM actively dissociates Salmonellatyphimurium σ28 RNA polymerase holoenzyme. Genes andDevelopment, 12(19), 3123–3136. https://doi.org/10.1101/gad.12.19.3123

  16. Chevance, F. & Hughes, K. (2008). Coordinating assemblyof a bacterial macromolecular machine. Nature ReviewsMicrobiology, 6(6), 455–465. https://doi.org/10.1038/nrmicro1887

  17. Chilcott, G. & Hughes, K. (2000). Coupling of Flagellar GeneExpression to Flagellar Assembly in Salmonella entericaSerovar Typhimurium and Escherichia coli. Microbiologyand Molecular Biology Reviews, 64(4), 694–708. https://doi.org/10.1128/mmbr.64.4.694-708.2000

  18. Claret, L. & Hughes, C. (2002). Interaction of the atypicalprokaryotic transcription activator FlhD2C2 with earlypromoters of the flagellar gene hierarchy. Journalof Molecular Biology, 321(2), 185–199. https://doi.org/10.1016/S0022-2836(02)00600-9

  19. Colland, F., Rain, J. C., Gounon, P., Labigne, A., Legrain, P. & DeReuse, H. (2001). Identification of the Helicobacter pylorianti-σ28 factor. Molecular Microbiology, 41(2), 477–487.https://doi.org/10.1046/j.1365-2958.2001.02537.x

  20. Davis, N. J. & Viollier, P. H. (2011). Probing flagellar promoteroccupancy in wild-type and mutant Caulobacter crescentusby chromatin immunoprecipitation. FEMS MicrobiologyLetters, 319(2), 146–152. https://doi.org/10.1111/j.1574-6968.2011.02275.x

  21. Dimmitt, K. & Simon, M. (1971). Purification and thermalstability of intact Bacillus subtilis flagella. Journal ofBacteriology, 105(1), 369–375. https://doi.org/10.1128/jb.105.1.369-375.1971

  22. Douillard, F., Ryan, K., Caly, D., Hinds, J., Witney, A., Husain,S. & O’Toole, P. (2008). Posttranscriptional regulation offlagellin synthesis in Helicobacter pylori by the RpoNchaperone HP0958. Journal of Bacteriology, 190(24),7975–7984. https://doi.org/10.1128/JB.00879-08

  23. Dugar, G., Svensson, S. L., Bischler, T., Wäldchen, S.,Reinhardt, R., Sauer, M. & Sharma, C. M. (2016). TheCsrA-FliW network controls polar localization of the dualfunctionflagellin mRNA in Campylobacter jejuni. NatureCommunications, 7(May), 1-18. https://doi.org/10.1038/ncomms11667

  24. Ely, B., Ely, T. W., Crymes, J. & Minnich, S. A. (2000). A family ofsix flagellin genes contributes to the Caulobacter crescentusflagellar filament. Journal of Bacteriology, 182(17), 5001–5004. https://doi.org/10.1128/JB.182.17.5001-5004.2000.

  25. England, J. C. & Gober, J. W. (2001). Cell cycle control ofcell morphogenesis in Caulobacter. Current Opinion inMicrobiology, 4(6), 674–680. https://doi.org/10.1016/S1369-5274(01)00268-5

  26. Ettema, T. J. & Andersson, S. G. (2009). The α-proteobacteria:The Darwin finches of the bacterial world. Biology Letters,5(3), 429–432. https://doi.org/10.1098/rsbl.2008.0793

  27. Ewing, C. P., Andreishcheva, E. & Guerry, P. (2009). Functionalcharacterization of flagellin glycosylation in Campylobacterjejuni 81-176. Journal of Bacteriology, 191(22), 7086–7093.https://doi.org/10.1128/JB.00378-09

  28. Faulds-Pain, A., Birchall, C., Aldridge, C., Smith, W., Grimaldi,G., Nakamura, S., Miyata, T., Gray, J., Li, G., Tang, J. X.,Namba, K., Minamino, T. & Aldridge, P. D. (2011). Flagellinredundancy in Caulobacter crescentus and its implicationsfor flagellar filament assembly. Journal of Bacteriology,193(11), 2695–2707. https://doi.org/10.1128/JB.01172-10

  29. Ferooz J., Lemaire J. & Letesson, J. (2011). Role of FlbT inflagellin production in Brucella melitensis. Microbiology,157, 1253-1262. https://doi: 10.1099/mic.0.044867-0.

  30. Frye, J., Karlinsey, J., Felise, H., Marzolf, B., Dowidar, N.,Mcclelland, M. & Hughes, K. (2006). Identification ofNew Flagellar Genes of Salmonella enterica. Journal ofBacteriology, 188(6), 2233–2243. https://doi.org/10.1128/JB.188.6.2233

  31. Gao, B., Lara-Tejero, M., Lefebre, M., Goodman, A. & Galán,J. (2014). Novel components of the flagellar system inepsilonproteobacteria. MBio, 5(3), 1–13. https://doi.org/10.1128/mBio.01349-14

  32. Gillen, K. & Hughes, K. (1991). Molecular characterizationof flgM, a gene encoding a negative regulator of flagellinsynthesis in Salmonella typhimurium. Journal ofBacteriology, 173(20), 6453–6459. https://doi.org/10.1128/jb.173.20.6453-6459.1991

  33. Gober, J. W. & Marques, M. V. (1995). Regulation ofcellular differentiation in Caulobacter crescentus.Microbiological Reviews, 59(1), 31–47. https://doi.org/10.1128/mmbr.59.1.31-47.1995

  34. Golden, N. & Acheson, D. (2002). Identification of motilityand autoagglutination Campylobacter jejuni mutants byrandom transposon mutagenesis. Infection and Immunity,70(4), 1761–1771. https://doi.org/10.1128/IAI.70.4.1761-1771.2002

  35. Goon, S., Ewing, C. P., Lorenzo, M., Pattarini, D., Majam,G. & Guerry, P. (2006). A ς28-regulated nonflagella genecontributes to virulence of Campylobacter jejuni 81-176.Infection and Immunity, 74(1), 769–772. https://doi.org/10.1128/IAI.74.1.769-772.2006

  36. Guerry, P., Ewing, C. P., Schirm, M., Lorenzo, M., Kelly,J., Pattarini, D., Majam, G., Thibault, P. & Logan,S. (2006). Changes in flagellin glycosylation affectCampylobacter autoagglutination and virulence. MolecularMicrobiology, 60(2), 299–311. https://doi.org/10.1111/j.1365-2958.2006.05100.x

  37. Gupta, R. S. (2006). Molecular signatures (unique proteinsand conserved indels) that are specific for the epsilonproteobacteria (Campylobacterales). BMC Genomics,7(August). https://doi.org/10.1186/1471-2164-7-167

  38. Helmann, J., Masiarz, F. & Chamberlin, M. (1988). Isolationand characterization of the Bacillus subtilis sigma 28 factor.Journal of Bacteriology, 170(4), 1560–1567. https://doi.org/10.1128/jb.170.4.1560-1567.1988

  39. Hendrixson, D., Akerley, B. & DiRita, V. (2001). Transposonmutagenesis of Campylobacter jejuni identifies a bipartiteenergy taxis system required for motility. MolecularMicrobiology, 40(1), 214–224. https://doi.org/10.1046/j.1365-2958.2001.02376.x

  40. Hendrixson, D. & DiRita, V.(2003). Transcription ofσ54-dependent but not σ 28-dependent flagellargenes in Campylobacter jejuni is associated withformation of the flagellar secretory apparatus. MolecularMicrobiology, 50(2), 687–702. https://doi.org/10.1046/j.1365-2958.2003.03731.x

  41. Hernández-Valle, J., Sanchez-Flores, A., Poggio, S., Dreyfus, G.& Camarena, L. (2020). The CtrA Regulon of Rhodobactersphaeroides Favors Adaptation to a Particular Lifestyle.Journal of Bacteriology, 202(7), 1–16. https://doi.org/10.1128/JB.00678-19

  42. Horstmann, J., Lunelli, M., Cazzola, H., Heidemann, J., Kühne,C., Steffen, P., Szefs, S., Rossi, C., Lokareddy, R., Wang,C., Lemaire, L., Hughes, K., Uetrecht, C., Schlüter, H.,Grassl, G., Stradal, T., Rossez, Y., Kolbe, M. & Erhardt, M.(2020). Methylation of Salmonella Typhimurium flagellapromotes bacterial adhesion and host cell invasion. NatureCommunications, 11(1), 1–11. https://doi.org/10.1038/s41467-020-15738-3

  43. Hughes, K., Gillen, K., Semon, M. & Karlinsey, J. (1993). Sensingstructural intermediates in bacterial flagellar assembly byexport of a negative regulator. Science, 262(5137), 1277–1280. https://doi.org/10.1126/science.8235660

  44. Josenhans, C., Vossebein, L., Friedrich, S. & Suerbaum, S.(2002). The neuA/flmD gene cluster of Helicobacterpylori is involved in flagellar biosynthesis and flagellinglycosylation. FEMS Microbiology Letters, 210(2),165–172. https://doi.org/10.1016/S0378-1097(02)00638-9

  45. Joslin, S. & Hendrixson, D. (2009). Activation of theCampylobacter jejuni FlgSR two-component systemis linked to the flagellar export apparatus. Journal ofBacteriology, 191(8), 2656–2667. https://doi.org/10.1128/JB.01689-08

  46. Karlinsey, J. E., Tsui, H., Winkler, M. & Hughes, K. (1998).Flk couples flgM translation to flagellar ring assembly inSalmonella typhimurium. Journal of Bacteriology, 180(20),5384–5397.https://doi.org/10.1128/jb.180.20.5384-5397.1998

  47. Klose, K. & Mekalanos, J. (1998). Differential regulationof multiple flagellins in Vibrio cholerae. Journal ofBacteriology, 180(2), 303–316. https://doi.org/10.1128/jb.180.2.303-316.1998

  48. Kobayashi, K. (2007). Gradual activation of the responseregulator DegU controls serial expression of genes forflagellum formation and biofilm formation in Bacillussubtilis. Molecular Microbiology, 66(2), 395–409. https://doi.org/10.1111/j.1365-2958.2007.05923.x

  49. Kutsukake, K., Ohya, Y. & Iino, T. (1990). Transcriptionalanalysis of the flagellar regulon of Salmonella typhimurium.Journal of Bacteriology, 172(2), 741–747. https://doi.org/10.1128/jb.172.2.741-747.1990

  50. Laub, M., Chen, S., Shapiro, L. & McAdams, H. (2002).Genes directly controlled by CtrA, a master regulatorof the Caulobacter cell cycle. Proceedings of theNational Academy of Sciences of the United States ofAmerica, 99(7), 4632–4637. https://doi.org/10.1073/pnas.062065699

  51. LaVallie, E. & Stahl, M. (1989). Cloning of the flagellin genefrom Bacillus subtilis and complementation studies of anin vitro-derived deletion mutation. Journal of Bacteriology,171(6), 3085–3094. https://doi.org/10.1128/jb.171.6.3085-3094.1989

  52. Lertsethtakarn, P., Ottemann, K. & Hendrixson, D. (2011).Motility and chemotaxis in Campylobacter andHelicobacter. Annual Review of Microbiology, 65, 389–410.https://doi.org/10.1146/annurev-micro-090110-102908

  53. Linton, D., Gilbert, M., Hitchen, P. G., Dell, A., Morris, H.R., Wakarchuk, W. W., Gregson, N. A. & Wren, B. W.(2000). Phase variation of a β-1,3 galactosyltransferaseinvolved in generation of the ganglioside GM1-like lipooligosaccharideof Campylobacter jejuni. MolecularMicrobiology, 37(3), 501–514. https://doi.org/10.1046/j.1365-2958.2000.02020.

  54. Llewellyn, M., Dutton, R., Easter, J., O’Donnol, D. & Gober,J. (2005). The conserved flaF gene has a critical role incoupling flagellin translation and assembly in Caulobactercrescentus. Molecular Microbiology, 57(4), 1127–1142.https://doi.org/10.1111/j.1365-2958.2005.04745.x

  55. Macnab, R. (2003). How Bacteria Assemble Flagella. AnnualReview of Microbiology, 57(1), 77–100. https://doi.org/10.1146/annurev.micro.57.030502.090832

  56. Mangan, E., Malakooti, J., Caballero, A., Ely, B., Gober, J. &Anderson, P. (1999). FlbT Couples Flagellum Assemblyto Gene Expression in Caulobacter crescentus. Journal ofBacteriology, 181(19), 6160–6170. https://doi.org/10.1128/JB.181.19.6160-6170.1999.

  57. McNally, D. J., Hui, J. P. M., Aubry, A. J., Mui, K. K. K.,Guerry, P., Brisson, J. R., Logan, S. M. & Soo, E. C.(2006). Functional characterization of the flagellarglycosylation locus in Campylobacter jejuni 81-176 usinga focused metabolomics approach. Journal of BiologicalChemistry, 281(27), 18489–1849. https://doi.org/10.1074/jbc.M603777200

  58. Michel, E., Mengaud, J., Galsworthy, S. & Cossart, P. (1998).Characterization of a large motility gene cluster containingthe cheR, motAB genes of Listeria monocytogenes andevidence that PrfA downregulates motility genes. FEMSMicrobiology Letters, 169(2), 341–347. https://doi.org/10.1016/S0378-1097(98)00498-4

  59. Minamino, T. & Macnab, R. (1999). Interactions amongcomponents of the Salmonella flagellar export apparatus andits substrates. Molecular Microbiology, 35(5), 1052–1064.https://doi.org/10.1046/j.1365-2958.2000.01771.x

  60. Muir, R. & Gober, J. (2001). Regulation of late flagellargene transcription and cell division by flagellumassembly in Caulobacter crescentus. MolecularMicrobiology, 41(1), 117–130. https://doi.org/10.1046/j.1365-2958.2001.02506.x

  61. Muir, R. & Gober, J. (2004). Regulation of FlbD activityby flagellum assembly is accomplished through directinteraction with the trans-acting factor, FliX. MolecularMicrobiology, 54(3), 715–730. https://doi.org/10.1111/j.1365-2958.2004.04298.x

  62. Mukherjee, S. & Kearns, D. (2014). The Structure andRegulation of Flagella in Bacillus subtilis. Annual Review ofGenetics, 48(1), 319–340. https://doi.org/10.1146/annurevgenet-120213-092406

  63. Mukherjee, S., Yakhnin, H., Kysela, D., Sokoloski, J.,Babitzke, P. & Kearns, D. (2011). CsrA-FliW interactiongoverns flagellin homeostasis and a checkpoint onflagellar morphogenesis in Bacillus subtilis. MolecularMicrobiology, 82(2), 447–461. https://doi.org/10.1111/j.1365-2958.2011.07822.x

  64. Ohnishi, K., Kutsukake, K., Suzuki, H. & Iino, T. (1990).Gene fliA encodes an alternative sigma factor specificfor flagellar operons in Salmonella typhimurium. MGGMolecular & General Genetics, 221(2), 139–147. https://doi.org/10.1007/BF00261713

  65. Patrick, J. & Kearns, D. (2009). Laboratory strains of Bacillussubtilis do not exhibit swarming motility. Journal ofBacteriology, 191(22), 7129–7133. https://doi.org/10.1128/JB.00905-09

  66. Poggio, S., Abreu-Goodger, C., Fabela, S., Osorio, A., Dreyfus,G., Vinuesa, P. & Camarena, L. (2007). A complete set offlagellar genes acquired by horizontal transfer coexistswith the endogenous flagellar system in Rhodobactersphaeroides. Journal of Bacteriology, 189(8), 3208–3216.https://doi.org/10.1128/JB.01681-06

  67. Poggio, S., Osorio, A., Dreyfus, G. & Camarena, L. (2005).The flagellar hierarchy of Rhodobacter sphaeroides iscontrolled by the concerted action of two enhancer-bindingproteins. Molecular Microbiology, 58(4), 969–983. https://doi.org/10.1111/j.1365-2958.2005.04900.x

  68. Power, P. & Jennings, M. (2003). The genetics of glycosylationin Gram-negative bacteria. FEMS MicrobiologyLetters, 218(2), 211–222. https://doi.org/10.1016/S0378-1097(02)01143-6

  69. Quon, K., Marczynski, G. & Shapiro, L. (1996). Cell cyclecontrol by an essential bacterial two-component signaltransduction protein. Cell, 84(1), 83–93. https://doi.org/10.1016/S0092-8674(00)80995-2

  70. Radomska, K., Ordoñez, S., Wösten, M., Wagenaar, J. & VanPutten, J. (2016). Feedback control of Campylobacterjejuni flagellin levels through reciprocal binding of FliWto flagellin and the global regulator CsrA. MolecularMicrobiology, 102(2), 207–220. https://doi.org/10.1111/mmi.13455

  71. Ramakrishnan, G. & Newton, A. (1990). FlbD of Caulobactercrescentus is a homologue of the NtrC (NRI) proteinand activates σ54-dependent flagellar gene promoters.Proceedings of the National Academy of Sciences of theUnited States of America, 87(6), 2369–2373. https://doi.org/10.1073/pnas.87.6.2369

  72. Ren, F., Lei, T., Song, Z., Yu, T., Li, Q., Huang, J. & Jiao,X. (2018). Could FlhF be a key element that controlsCampylobacter jejuni flagella biosynthesis in the initialassembly stage? Microbiological Research, 207, 240–248.https://doi.org/10.1016/j.micres.2017.12.006

  73. Romilly, C., Hoekzema, M., Holmqvist, E. & Wagner, E. (2020).Small RNAs OmrA and OmrB promote class III flagellargene expression by inhibiting the synthesis of anti-Sigmafactor FlgM. RNA Biology, 17(6), 872–880. https://doi.org/10.1080/15476286.2020.1733801

  74. Rust, M., Borchert, S., Niehus, E., Kuehne, S., Gripp, E.,Bajceta, A., McMurry, J., Suerbaum, S., Hughes, K.& Josenhans, C. (2009). The Helicobacter pylori antisigmafactor FlgM is predominantly cytoplasmic andcooperates with the flagellar basal body protein FlhA.Journal of Bacteriology, 191(15), 4824–4834. https://doi.org/10.1128/JB.00018-09

  75. Schaubach, O. & Dombroski, A. (1999). Transcription initiationat the flagellin promoter by RNA polymerase carryingσ28 from Salmonella typhimurium. Journal of BiologicalChemistry, 274(13), 8757–8763. https://doi.org/10.1074/jbc.274.13.8757

  76. Schirm, M., Soo, E., Aubry, A., Austin, J., Thibault, P. & Logan,S. (2003). Structural, genetic and functional characterizationof the flagellin glycosylation process in Helicobacter pylori.Molecular Microbiology, 48(6), 1579–1592. https://doi.org/10.1046/j.1365-2958.2003.03527.x

  77. Serizawa, M., Yamamoto, H., Yamaguchi, H., Fujita, Y.,Kobayashi, K., Ogasawara, N. & Sekiguchi, J. (2004).Systematic analysis of SigD-regulated genes in Bacillussubtilis by DNA microarray and Northern blotting analyses.Gene, 329(1–2), 125–136. https://doi.org/10.1016/j.gene.2003.12.024

  78. Shelswell, K. J., Taylor, T. & Beatty, J. T. (2005).Photoresponsive flagellum-independent motility of thepurple phototrophic bacterium Rhodobacter capsulatus.Journal of Bacteriology, 187(14), 5040–5043. https://doi.org/10.1128/JB.187.14.5040-5043.2005

  79. Smith, T. & Hoover, T. R. (2009). Chapter 8 DecipheringBacterial Flagellar Gene Regulatory Networks in theGenomic Era. En Laskin, A., Sariaslani, S. & Gadd G.(Ed). Advances in Applied Microbiology (1st ed., Vol.67, Issue C). Elsevier Inc. https://doi.org/10.1016/S0065-2164(08)01008-3

  80. Soutourina, O. & Bertin, P. (2003). Regulation cascade offlagellar expression in Gram-negative bacteria. FEMSMicrobiology Reviews, 27(4), 505–523. https://doi.org/10.1016/S0168-6445(03)00064-0

  81. Tasteyre, A., Barc, M. C., Karjalainen, T., Dodson, P., Hyde, S.,Bourlioux, P. & Borriello, P. (2000). A Clostridium difficilegene encoding flagellin. Microbiology, 146(4), 957–966.https://doi.org/10.1099/00221287-146-4-957

  82. Wang, F., Burrage, A., Postel, S., Clark, R., Orlova, A., Sundberg,E., Kearns, D. & Egelman, E. (2017). A structural modelof flagellar filament switching across multiple bacterialspecies. Nature Communications, 8(1). https://doi.org/10.1038/s41467-017-01075-5

  83. Wang, H., Ziesche, L., Frank, O., Michael, V., Martin, M.,Petersen, J., Schulz, S., Wagner-Döbler, I. & Tomasch, J.(2014). The CtrA phosphorelay integrates differentiationand communication in the marine alphaproteobacteriumDinoroseobacter shibae. BMC Genomics, 15(1), 1–17.https://doi.org/10.1186/1471-2164-15-130

  84. Wösten, M., Van Dijk, L., Veenendaal, A., De Zoete,M., Bleumink-Pluijm, N. & Van Putten, J. (2010).Temperature-dependent FlgM/FliA complex formationregulates Campylobacter jejuni flagella length. MolecularMicrobiology, 75(6), 1577–1591. https://doi.org/10.1111/j.1365-2958.2010.07079.x

  85. Wösten, M., Wagenaar, J. & Van Putten, J. (2004). The FlgS/FlgRTwo-component Signal Transduction System Regulates thefla Regulon in Campylobacter jejuni. Journal of BiologicalChemistry, 279(16), 16214–16222.https://doi.org/10.1074/jbc.M400357200

  86. Xu, Z., Dutton, R. J. & Gober, J. W. (2011). Direct interactionof FliX and FlbD is required for their regulatory activityin Caulobacter crescentus. BMC Microbiology, 11. https://doi.org/10.1186/1471-2180-11-89

  87. Yakhnin, H., Pandit, P., Petty, T. J., Baker, C. S., Romeo, T.& Babitzke, P. (2007). CsrA of Bacillus subtilis regulatestranslation initiation of the gene encoding the flagellinprotein (hag) by blocking ribosome binding. MolecularMicrobiology, 64(6), 1605–1620. https://doi.org/10.1111/j.1365-2958.2007.05765.x

  88. Wiggs, J. L., Gilman, M. Z. & Chamberlin, M. J. (1981).Heterogeneity of RNA polymerase in Bacillus subtilis:evidence for an additional sigma factor in vegetative cells.Proceedings of the National Academy of Sciences of theUnited States of America, 78(5), 2762–2766. https://doi.org/10.1073/pnas.78.5.2762




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